- Email: [email protected]
Series of Noncontrast Time-of-Flight Magnetic Resonance Angiographies to Identify Problems with Arteriovenous Fistula Maturation
Accepted Manuscript Series of Non-Contrast Time of Flight MRAs to Identify Problems with AVF Maturation LCDR Aaron J. Gonzalez, DO, CDR(s) Kevin M. Casey, MD, FACS, LCDR Benjamin J. Drinkwine, MD, CAPT Jeffrey S. Weiss, MD, FACS PII:
S0890-5096(15)00600-7
DOI:
10.1016/j.avsg.2015.07.005
Reference:
AVSG 2484
To appear in:
Annals of Vascular Surgery
Received Date: 20 March 2015 Revised Date:
7 July 2015
Accepted Date: 15 July 2015
Please cite this article as: Gonzalez AJ, Casey KM, Drinkwine BJ, Weiss JS, Series of Non-Contrast Time of Flight MRAs to Identify Problems with AVF Maturation, Annals of Vascular Surgery (2015), doi: 10.1016/j.avsg.2015.07.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
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Series of Non-Contrast Time of Flight MRAs to Identify Problems with AVF Maturation
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1. Department of Radiology Division of Interventional Radiology Naval Medical Center San Diego 34800 Bob Wilson Drive San Diego, CA 92134
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LCDR Aaron J Gonzalez, DO1, CDR(s) Kevin M Casey, MD, FACS2, LCDR Benjamin J Drinkwine, MD1, CAPT Jeffrey S Weiss, MD, FACS2
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2. Department of General Surgery Division of Vascular Surgery Naval Medical Center San Diego 34800 Bob Wilson Drive San Diego, CA 92134
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Corresponding author: Jeffrey S Weiss
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Naval Medical Center San Diego
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34800 Bob Wilson Drive, San Diego, CA 92134
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Personal cell phone: 619-342-5410
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Work phone: 619-532-7578
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Work email: [email protected]
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Fax: 619-532-7673
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Disclaimer: The views expressed in this manuscript are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, the Department of Defense, or the United States Government.
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Series of Non-Contrast Time of Flight MRAs to Identify Problems with AVF Maturation
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Methods: Consecutive patients with abnormal findings on CDUS or physical examination following AVF creation underwent 3 dimensional (3-D) TOF-MR. Imaging was performed at 3 Tesla with a scan acquisition time of approximately 15 minutes. The technique was similar to head and neck MRA, except pre-saturation bands were not used, thereby allowing simultaneous visualization of both arterial and venous flow. A total of 19 TOF-MR studies were performed.
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Results: Nineteen patients underwent imaging and were the focus of this study. 17/19 TOF-MR studies were of diagnostic quality and yielded findings which enabled the vascular surgeon to take corrective measures. Findings included inflow stenosis, anastomotic narrowing, venous outflow stenosis, and hemodynamically significant venous tributaries. 12/17 patients required conventional digital subtraction angiography (DSA). The congruence rate between TOF-MR and DSA was 83.3%. Four patients (21%) avoided DSA and went directly to definitive surgical treatment including branch ligation (3) or new access (1).
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Background: Successful maturation of arteriovenous fistulas (AVFs) remains a challenge for those managing patients with end stage renal disease. Time of flight magnetic resonance angiography (TOF-MR) can be employed to evaluate AVFs without the risk of radiation exposure, intravenous contrast, or reliance on the operator-dependent modality of color-flow duplex ultrasonography (CDUS). The objective of our study was to assess the utility of TOF-MR in the evaluation of non-maturing AVFs and to identify the best clinical situations to employ this technology.
Conclusions: This is the first report in the literature of successful implementation of 3-D TOFMR to assist in identifying AVF maturation problems. This unique non-invasive imaging modality provides actionable images without contrast or radiation exposure and can obviate the need for invasive diagnostic procedures or provide an anatomic map for planning corrective intervention.
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Introduction
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It is estimated that 400,000 individuals with end-stage renal disease (ESRD) are on hemodialysis in the United States, leading to an annual cost of over $3 billion for creating and maintaining arteriovenous access. Considerable time and expense is devoted to both the creation and maintenance of arteriovenous access for hemodialysis. In an effort to improve patient outcomes and quality of life, the Kidney Dialysis Outcome Quality Initiative guidelines1 and the National Vascular Access Improvement Initiative promulgated the Fistula First initiative, resulting in an increase in the percentage of AVFs created in the United States. Autogenous AVFs have demonstrated better patency and lower intervention and infection rates when compared to arteriovenous grafts (AVGs).2 Nonetheless, reported non-maturation rates of up to 30%3 remain a concern.
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In addition to physical exam, color Doppler ultrasound (CDUS) has become the primary imaging modality to assess maturity.4,5 CDUS is non-invasive, reproducible, and inexpensive. The main limitation to this modality is that it is operator-dependent with accuracy rates that vary in the literature from 50-81%.6,7 It may also be difficult to interpret, thus requiring patients to undergo angiography to elucidate the cause for non-maturation. Catheter angiography carries risks of ionizing radiation, conscious sedation, and contrast exposure for a patient population with severely depressed GFR, increasing the risk of progressive renal dysfunction from contrastinduced nephropathy (CIN).
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Magnetic resonance angiography (MRA) was introduced as a method for evaluating AVF as early as 1991,8,9 but was largely abandoned secondary to inadequate image quality. Previous MRA studies also relied on intravenous gadolinium administration for vascular imaging, exposing patients with renal failure to the potentially fatal nephrogenic systemic fibrosis. Technological advances, including higher field strength magnets and improved computer data processing capabilities now allow acquisition of high quality images of vascular anatomy using a non-contrast 3D TOF-MR technique.
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The objective of our study was to assess the utility of 3-D TOF-MR in the work-up of nonmaturing AVFs. We also sought to identify the best clinical situations to employ this technology.
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Materials and Methods
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The study was a retrospective, single-institution analysis of 19 patients who underwent TOF-MR for the evaluation of non-maturing AVFs at Naval Medical Center San Diego from April 2013 to June 2014. Data was obtained by direct chart abstraction. Patient consent was obtained prior to any invasive procedure. The study was approved through the local Investigative Review Board as a performance improvement project.
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All patients underwent TOF-MR with a Philips Ingenia 3.0T MRI scanner (Philips Healthcare; Best, The Netherlands). TOF-MR is a non-contrast angiographic technique which generates images based on flow related signal. A 16-channel torso array receiver coil was used with the patient’s arm in the iso-center of the magnetic bore to reduce imaging artifact. Similar to head and neck TOF-MR examinations, the applied saturation pulses null the stationary protons within the soft tissues, allowing visualization of flowing blood. The pre-saturation bands typically used in head and neck imaging were omitted in our studies to allow simultaneous visualization of both arterial and venous blood flow. The images were acquired in three separate slabs which were then combined to create 3-D Mobiview images of the vasculature. The reconstruction voxel size was 0.5 x 0.5 x 0.8 mm and the acquired matrix size was 400 x 250, creating images with high spatial resolution. The high contrast resolution between flowing blood and stationary tissue allows creation of tissue subtracted 3-D images of the vasculature. The scan time was between 15 and 20 minutes per patient.
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Patients were routinely evaluated per the vascular surgery department clinical practice guidelines with physical examination at 2 weeks followed by physical examination and/or CDUS 10 weeks after AVF creation. The indications for TOF-MR were abnormal physical examination or duplex findings that indicated a significant stenosis, vein diameter < 5mm, or flow < 500 ml/min.10 Each vascular surgeon independently determined which AVF was at risk for nonmaturation and decided which patient went on to have a TOF-MR.
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Results
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Nineteen patients over 15 months had autogenous AVFs with subsequent abnormal physical examination or ultrasound findings. The median patient age was 65.9 (range, 52-84 years). Nine patients were male and 10 patients were female. Sixteen patients had radiocephalic AVFs and three had brachiocephalic AVFs. Sixteen of the nineteen patients were diabetic. Eight patients were already on hemodialysis during the evaluation and work-up of their AVF non-maturation.
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DSA and TOF-MR images were interpreted by both a radiologist and a vascular surgeon. While the images were reviewed and discussed in a multidisciplinary setting, the final written report was used for the purposes of this study. CDUS studies were performed by a specialized vascular technician and interpreted by a vascular surgeon; the final written report was used for the purposes of this study. At our institution, we define successful use of a mature fistula after completing six consecutive hemodialysis runs.
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The overall AVF maturation rate for the cohort was 82%. Ten patients underwent successful percutaneous transluminal angioplasty (PTA). Three patients needed a subsequent cephalic branch ligation. One patient underwent both.
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Seven patients with TOF-MR did not have a subsequent DSA (Table 3). Three patients went directly to operative intervention rather than angiography. All three had accessory cephalic vein branch ligation under local anesthesia and one patient had a duplex-directed PTA; all of these AVF went on to maturation and successful cannulation. Three AVFs were deemed nonsalvageable based on TOF-MR and clinical findings. Two were revised to new accesses and 1 was abandoned as the patient elected for peritoneal dialysis. Two studies were considered nondiagnostic at the time of interpretation. In these two cases, the flow related signal within the vessels was insufficient to produce adequate images. This likely represented failing AVFs with low-flow states that could have been predictive of a non-salvageable AVF. One patient was lost to follow-up.
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All 19 patients in our study had TOF-MRs performed (Table 1). Twelve patients went on to have a conventional catheter angiogram, allowing for intermodality comparison. The congruence rate between the two modalities was 83.3% (Table 2). Cases in which the final report agreed and led to the same intervention were considered congruent. There were 2 false positives identified. In each case the MR overestimated the degree of stenosis.
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Discussion
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This study demonstrated the novel implementation of 3-D TOF-MR in the evaluation of AVF maturation. We found this modality to be useful in avoiding an unnecessary DSA in 21% of our patients. The MRA findings on 4 out of the 19 patients provided information that avoided a diagnostic angiogram. Three of these patients went on to branch ligation without angiogram, and one patient’s AVF was abandoned after MRA showed severe narrowing versus occlusion of the vein. This imaging possessed additional qualitative benefits to other patients, which aided in better case planning, lower radiation exposure, and decreased intravenous contrast amounts. These are similar subjective findings described by Cavagna, et al. in their utilization of MRA on 13 patients with AVF non-maturation.11 The 3-D images provide vessel visualization in multiple planes with a single non-invasive acquisition. We believe this technique delineates the anatomy well and offers several advantages over catheter directed angiography. MR-TOF can obviate the need for invasive access and repeated angiographic runs in multiple planes which frequently leads to increased contrast administration and prolonged radiation exposure.12
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When analyzing CDUS with respect to DSA, the congruence rate was 62%. Reasons for discordant findings included failure to identify the precise location of a stenosis (N = 4) and an unidentified accessory vein branch (N = 1).
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Many studies have shown MRA to benefit in subsequent case planning.13-15 We also found that TOF-MR commonly provided radiologic images that aided in our case preparation. Ten of 12 patients in our group went on to have an angiogram that illustrated concordant findings. The 5
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CDUS remains a valuable tool in the armamentarium of AVF evaluation. However, significant limitations exist, resulting from operator dependence, lack of 3D acquisition, and difficulty displaying complex anatomic and spatial relationships on static images. Sonographic examinations are often limited to the region near the AVF and can miss lesions that the larger field of view obtained with TOF-MR can visualize. Similar to the findings noted by Zhang et al,12 we found that the increased field of view with MRI has tremendous value in evaluating abnormalities that may be more remote than typically identified. One patient in our series had a radial artery stenosis located 10 cm proximal to the anastomosis that was visualized with TOFMR and later treated with conventional angiogram (Figure 2). This lesion would have been likely missed on a standard protocol CDUS.
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TOF-MR can also clarify areas of concern on CDUS and potentially obviate the need for angiography altogether. Two patients had an anastomotic stenosis and several competing veins identified on CDUS. However, subsequent TOF-MR showed the competing veins but no stenosis (Figure 3). If treatment had been based solely on CDUS, both of these patients would have undergone an unnecessary diagnostic angiogram. Instead, both patients underwent venous branch ligation and are now using their AVFs successfully without the need to perform an angiogram.
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There is currently no cost information for AVF TOF-MR, but extrapolating carotid TOF-MR, we estimate it to be about twice the cost of CDUS and one third that of a diagnostic angiogram based on current CHAMPUS National Pricing System reimbursement amounts. Obtaining MRA TOF on all patients prior to intervention is not a cost-effective strategy. Independent of where the DSA is performed, the goals of TOF-MR are to identify cases that could be surgically correctable without DSA, identify potentially non-salvageable AVF, and provide preoperative case-planning for challenging anatomic cases. Further studies designed to refine the criteria that would prompt TOF-MR are needed. Our ultimate goal is to reduce the number of invasive diagnostic procedures while at the same time minimizing unnecessary duplicative diagnostic imaging.
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pre-procedure MRA frequently allowed for decreased contrast administration and immediate lesion identification. One TOF-MR found a venous stenosis that was used as a roadmap to guide percutaneous intervention without the need for contrast administration during venoplasty (Figure 1). We discovered that the TOF-MR frequently provided an anatomic overview which helped plan access site locations near areas of stenosis or served as an anatomic map for future branch vessel ligation.
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During our study, we recognized several limitations of TOF-MR. One potential diagnostic pitfall is the overestimation of the degree of stenosis. Stagnant blood or blood flowing in the same plane as the image acquisition (Figure 4) can also appear as an area of stenosis. Knowledge of 6
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this artifact and interpretation adjustments can mitigate false positive findings on these studies. Relative insensitivity to low flow states can also be a limitation with 3D TOF-MR. Future studies could include 2D TOF-MR in cases were low blood flow is suspected to be the cause for inadequate flow related signal production within vessels. Additionally, velocity and flow rate measurements are currently best obtained with CDUS, but newer phase contrast techniques may offer a promising future for MRI into the physiologic assessment arena. Lastly, given current financial constraints, technological limitations, and the difficulties of treating this chronic population, a pertinent question from this series remains the most appropriate implementation of TOF-MR. We do not argue that every patient warrants this modality following AVF creation. However, our 82% maturation rate in a small study group deemed “at risk” does suggest that there is a role for this in assisting with AVF maturation.
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Conclusion
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3D TOF-MR appears to have significant utility in the evaluation and management of AVF maturation. In addition to demonstrating a high congruence rate with DSA, we found that 21% of patients were spared an unnecessary diagnostic angiogram due to the information provided by TOF-MR. We also felt that, in cases where therapeutic angiogram was indicated, the contrast load and radiation dose was significantly reduced by having a pre-procedure TOF-MR roadmap. Further studies focusing on patient subsets that benefit from TOF-MR will help refine patient selection and may reduce overall costs.
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Our study has several inherent limitations, including the small sample size, single institutional practice, retrospective nature, and qualitative nature. Because we chose to investigate all AVFs which were considered to be at risk for non-maturation, we do not know what the natural history was of this cohort were we not to intervene. However, our results demonstrated that 3D TOF-MR is a feasible imaging modality that has added value in the evaluation of AVF maturation, especially in pre-dialysis patients where contrast exposure is an issue.
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Figure Legends:
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Figure 1. A) TOF-MR image showing tandem stenosis of proximal outflow vein. B and C) DSA with PTA of tandem venous stenosis without intravenous iodinated contrast administration (the contrast is only present within the angioplasty balloon).
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Figure 3. A) TOF-MR image showing a large competing venous branch.
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Figure 4. A) TOF-MR showing an area of decreased signal at the anastomosis interpreted as an area of stenosis. This is a common area of signal loss seen where blood is flowing in the same plane as the image acquisition. B) DSA image showing no significant stenosis.
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Figure 2. A) TOF-MR image showing a proximal arterial stenosis. B) DSA confirming a proximal arterial stenosis.
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Table 1. Patient listing with modality findings and outcomes
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Table 2. 12 cases with TOF-MR and comparison DSA
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Table 3. Outcome of the 7 cases where TOF-MR had no comparison DSA
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References:
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Patel ST, Hughes J, Mills JL. Failure of arteriovenous fistula maturation: An unintended consequence of exceeding Dialysis Outcome Quality Initiative guidelines for hemodialysis access. J Vasc Surg 2003;38:439-45. 4
Doelman C, Duijm LE, Liem YS, et al. Stenosis detection in failing hemodialysis access fistulas and grafts: Comparison of color doppler ultrasonography, contrast-enhanced magnetic resonance angiography, and digital subtraction angiography. J Vasc Surg 2005;42:739-46.
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Ascher E, Gade P, Hingorani A, et al. Changes in the practice of angioaccess surgery: Impact of dialysis outcome and quality initiative recommendations. J Vasc Surg 2000;31:84-92.
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Dumars MC, Thompson WE, Bluth EI, et al. Management of suspected hemodialysis graft dysfunction: Usefulness of diagnostic US. Radiology 2002;222:103-7. 6
Tordoir JH, DeBruin HG, Hoeneveld H, et al. Duplex ultrasound scanning in the assessment of arteriovenous fistulas created for hemodialysis access: Comparison with digital subtraction angiography. J Vasc Surg 1989; 10: 122-8. 7
Middleton WD, Picus DD, Marx MV, et al. Color Doppler sonography of hemodialysis vascular access: Comparison with angiography. Am J Roentgenol 1989; 152: 633-39. 8
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Waldman GJ, Pattynama PM, Chang PC, et al. Magnetic resonance angiography of dialysis access shunts: Initial results. Magn Reson Imaging 1996; 14(2):197-200. 9
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Konermann M, Sanner B, Laufer U, et al. Magnetic resonance angiography as a technique for the visualization of hemodialysis shunts. Nephron 1996;73:73-8. 10
Robbin ML, Chamberlain NE, Lockhart ME, et al. Hemodialysis arteriovenous fistula maturity: US evaluation. Radiology 2002;225:59-64. 11
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National Kidney Foundation. K/DOQI clinical practice guidelines for vascular access, 2000. Am J Kidney Dis 2001;37:S137-S81.
Cavagna E, D’Andrea P, Schiavon F, et al. Failing hemodialysis arteriovenous fistula and percutaneous treatment: imaging with CT, MRI and digital subtraction angiography. Cardiovasc Intervent Radiol 2000;23:262-5. 12
Zhang J, Hecht E, Maldonado T, et al. Time-resolved 3D angiography with parallel imaging for evaluation of hemodialysis fistula and grafts: Initial experience. Am J Roentgenol 2006;186:1436-42.
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Froger CL, Duijm LE, Liem YS, et al. Stenosis detection with MR angiography and digital subtraction angiography in dysfunctional hemodialysis access fistulas and grafts. Radiology 2005;234:284-91. 15
Planken RN, Tordoir JH, Dammers R, et al. Stenosis detection in forearm hemodialysis arteriovenous fistulae by multiphase contrast-enhanced magnetic resonance angiography: Preliminary experience. J Magn Reson 2003;17:54-64.
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Smits JH, Bos C, Elgersma OE, et al. Hemodialysis access imaging: Comparison of flowinterrupted contrast-enhanced MR angiography and digital subtraction angiography. Radiology 2002;225:829-34.
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Angiogram / Intervention Anastomotic & venous stenosis / PTA Branch ligation Unremarkable Venous stenosis N/A Venous stenosis & competing vein / PTA & branch ligation Anastomotic & venous stenosis / PTA N/A PTA & Branch ligation in OR N/A Branch ligation Competing vein / branch ligation Anastomotic stenosis / PTA Venous stenosis / PTA Venous & arterial stenosis / PTA Venous stenosis / PTA N/A Anastomotic stenosis & competing vein / PTA Thrombosis AVF / tPA & PTA
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Time-of-Flight MR Anastomotic & venous stenosis Competing veins Anastomotic stenosis Venous stenosis Non-diagnostic exam Venous stenosis Anastomotic & venous stenosis Venous stenosis & competing veins Venous stenosis & competing veins Non-diagnostic exam Competing veins Venous stenosis & competing vein Anastomotic stenosis Venous stenosis Venous & arterial stenosis Venous stenosis Severe narrowing vs occlusion of vein Anastomotic stenosis & competing vein Venous stenosis
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Color-flow Duplex Ultrasound Arterial stenosis Arterial stenosis & competing vein Low flow Anastomotic stenosis Anastomotic stenosis & competing veins N/A Venous stenosis Anastomotic stenosis Competing veins & low flow N/A Anastomotic stenosis & competing veins Anastomotic stenosis Proximal venous stenosis Venous stenosis Venous & arterial stenosis Venous stenosis N/A Anastomotic stenosis & competing vein N/A
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Table 1. Patient listing with modality findings and outcomes
Outcome Mature Successful use Mature Pt expired New access Successful use Successful use Lost to f/u Mature New access Successful use Mature Mature Successful use Successful use Successful use Abandoned Successful use Successful use
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Table 2. 12 cases with TOF-MR and comparison DSA
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Angiogram Same Same Same Same Same Same Same Same Same Thrombosis AVF Competing vein Unremarkable
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Time-of-Flight Magnetic Resonance Anastomotic & venous stenosis Venous stenosis Venous stenosis & competing veins Anastomotic & venous stenosis Anastomotic stenosis Venous stenosis Venous & arterial stenosis Venous stenosis Anastomotic stenosis & competing vein Venous stenosis Venous stenosis & competing vein Anastomotic stenosis
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Outcome Mature Pt expired Mature Successful use Mature Successful use Successful use Successful use Successful use Successful use Mature Mature
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Table 3. Outcome of the 7 cases where TOF-MR had no comparison DSA
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Intervention Branch ligation (OR) PTA & branch ligation (OR) Branch ligation (OR) N/A N/A N/A N/A
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Time-of-Flight Magnetic Resonance Competing veins Venous stenosis & competing veins Competing veins Severe narrowing vs occlusion of vein Non-diagnostic exam Non-diagnostic exam Venous stenosis & competing veins
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Outcome Successful use Successful use Successful use Peritoneal dialysis New access New access Lost to follow-up
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S0890-5096(15)00600-7
DOI:
10.1016/j.avsg.2015.07.005
Reference:
AVSG 2484
To appear in:
Annals of Vascular Surgery
Received Date: 20 March 2015 Revised Date:
7 July 2015
Accepted Date: 15 July 2015
Please cite this article as: Gonzalez AJ, Casey KM, Drinkwine BJ, Weiss JS, Series of Non-Contrast Time of Flight MRAs to Identify Problems with AVF Maturation, Annals of Vascular Surgery (2015), doi: 10.1016/j.avsg.2015.07.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
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Series of Non-Contrast Time of Flight MRAs to Identify Problems with AVF Maturation
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1. Department of Radiology Division of Interventional Radiology Naval Medical Center San Diego 34800 Bob Wilson Drive San Diego, CA 92134
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LCDR Aaron J Gonzalez, DO1, CDR(s) Kevin M Casey, MD, FACS2, LCDR Benjamin J Drinkwine, MD1, CAPT Jeffrey S Weiss, MD, FACS2
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2. Department of General Surgery Division of Vascular Surgery Naval Medical Center San Diego 34800 Bob Wilson Drive San Diego, CA 92134
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Corresponding author: Jeffrey S Weiss
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Naval Medical Center San Diego
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34800 Bob Wilson Drive, San Diego, CA 92134
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Personal cell phone: 619-342-5410
22
Work phone: 619-532-7578
23
Work email: [email protected]
24
Fax: 619-532-7673
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Disclaimer: The views expressed in this manuscript are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, the Department of Defense, or the United States Government.
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Series of Non-Contrast Time of Flight MRAs to Identify Problems with AVF Maturation
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Methods: Consecutive patients with abnormal findings on CDUS or physical examination following AVF creation underwent 3 dimensional (3-D) TOF-MR. Imaging was performed at 3 Tesla with a scan acquisition time of approximately 15 minutes. The technique was similar to head and neck MRA, except pre-saturation bands were not used, thereby allowing simultaneous visualization of both arterial and venous flow. A total of 19 TOF-MR studies were performed.
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Results: Nineteen patients underwent imaging and were the focus of this study. 17/19 TOF-MR studies were of diagnostic quality and yielded findings which enabled the vascular surgeon to take corrective measures. Findings included inflow stenosis, anastomotic narrowing, venous outflow stenosis, and hemodynamically significant venous tributaries. 12/17 patients required conventional digital subtraction angiography (DSA). The congruence rate between TOF-MR and DSA was 83.3%. Four patients (21%) avoided DSA and went directly to definitive surgical treatment including branch ligation (3) or new access (1).
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Background: Successful maturation of arteriovenous fistulas (AVFs) remains a challenge for those managing patients with end stage renal disease. Time of flight magnetic resonance angiography (TOF-MR) can be employed to evaluate AVFs without the risk of radiation exposure, intravenous contrast, or reliance on the operator-dependent modality of color-flow duplex ultrasonography (CDUS). The objective of our study was to assess the utility of TOF-MR in the evaluation of non-maturing AVFs and to identify the best clinical situations to employ this technology.
Conclusions: This is the first report in the literature of successful implementation of 3-D TOFMR to assist in identifying AVF maturation problems. This unique non-invasive imaging modality provides actionable images without contrast or radiation exposure and can obviate the need for invasive diagnostic procedures or provide an anatomic map for planning corrective intervention.
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Introduction
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It is estimated that 400,000 individuals with end-stage renal disease (ESRD) are on hemodialysis in the United States, leading to an annual cost of over $3 billion for creating and maintaining arteriovenous access. Considerable time and expense is devoted to both the creation and maintenance of arteriovenous access for hemodialysis. In an effort to improve patient outcomes and quality of life, the Kidney Dialysis Outcome Quality Initiative guidelines1 and the National Vascular Access Improvement Initiative promulgated the Fistula First initiative, resulting in an increase in the percentage of AVFs created in the United States. Autogenous AVFs have demonstrated better patency and lower intervention and infection rates when compared to arteriovenous grafts (AVGs).2 Nonetheless, reported non-maturation rates of up to 30%3 remain a concern.
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In addition to physical exam, color Doppler ultrasound (CDUS) has become the primary imaging modality to assess maturity.4,5 CDUS is non-invasive, reproducible, and inexpensive. The main limitation to this modality is that it is operator-dependent with accuracy rates that vary in the literature from 50-81%.6,7 It may also be difficult to interpret, thus requiring patients to undergo angiography to elucidate the cause for non-maturation. Catheter angiography carries risks of ionizing radiation, conscious sedation, and contrast exposure for a patient population with severely depressed GFR, increasing the risk of progressive renal dysfunction from contrastinduced nephropathy (CIN).
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Magnetic resonance angiography (MRA) was introduced as a method for evaluating AVF as early as 1991,8,9 but was largely abandoned secondary to inadequate image quality. Previous MRA studies also relied on intravenous gadolinium administration for vascular imaging, exposing patients with renal failure to the potentially fatal nephrogenic systemic fibrosis. Technological advances, including higher field strength magnets and improved computer data processing capabilities now allow acquisition of high quality images of vascular anatomy using a non-contrast 3D TOF-MR technique.
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The objective of our study was to assess the utility of 3-D TOF-MR in the work-up of nonmaturing AVFs. We also sought to identify the best clinical situations to employ this technology.
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Materials and Methods
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The study was a retrospective, single-institution analysis of 19 patients who underwent TOF-MR for the evaluation of non-maturing AVFs at Naval Medical Center San Diego from April 2013 to June 2014. Data was obtained by direct chart abstraction. Patient consent was obtained prior to any invasive procedure. The study was approved through the local Investigative Review Board as a performance improvement project.
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All patients underwent TOF-MR with a Philips Ingenia 3.0T MRI scanner (Philips Healthcare; Best, The Netherlands). TOF-MR is a non-contrast angiographic technique which generates images based on flow related signal. A 16-channel torso array receiver coil was used with the patient’s arm in the iso-center of the magnetic bore to reduce imaging artifact. Similar to head and neck TOF-MR examinations, the applied saturation pulses null the stationary protons within the soft tissues, allowing visualization of flowing blood. The pre-saturation bands typically used in head and neck imaging were omitted in our studies to allow simultaneous visualization of both arterial and venous blood flow. The images were acquired in three separate slabs which were then combined to create 3-D Mobiview images of the vasculature. The reconstruction voxel size was 0.5 x 0.5 x 0.8 mm and the acquired matrix size was 400 x 250, creating images with high spatial resolution. The high contrast resolution between flowing blood and stationary tissue allows creation of tissue subtracted 3-D images of the vasculature. The scan time was between 15 and 20 minutes per patient.
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Patients were routinely evaluated per the vascular surgery department clinical practice guidelines with physical examination at 2 weeks followed by physical examination and/or CDUS 10 weeks after AVF creation. The indications for TOF-MR were abnormal physical examination or duplex findings that indicated a significant stenosis, vein diameter < 5mm, or flow < 500 ml/min.10 Each vascular surgeon independently determined which AVF was at risk for nonmaturation and decided which patient went on to have a TOF-MR.
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Results
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Nineteen patients over 15 months had autogenous AVFs with subsequent abnormal physical examination or ultrasound findings. The median patient age was 65.9 (range, 52-84 years). Nine patients were male and 10 patients were female. Sixteen patients had radiocephalic AVFs and three had brachiocephalic AVFs. Sixteen of the nineteen patients were diabetic. Eight patients were already on hemodialysis during the evaluation and work-up of their AVF non-maturation.
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DSA and TOF-MR images were interpreted by both a radiologist and a vascular surgeon. While the images were reviewed and discussed in a multidisciplinary setting, the final written report was used for the purposes of this study. CDUS studies were performed by a specialized vascular technician and interpreted by a vascular surgeon; the final written report was used for the purposes of this study. At our institution, we define successful use of a mature fistula after completing six consecutive hemodialysis runs.
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The overall AVF maturation rate for the cohort was 82%. Ten patients underwent successful percutaneous transluminal angioplasty (PTA). Three patients needed a subsequent cephalic branch ligation. One patient underwent both.
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Seven patients with TOF-MR did not have a subsequent DSA (Table 3). Three patients went directly to operative intervention rather than angiography. All three had accessory cephalic vein branch ligation under local anesthesia and one patient had a duplex-directed PTA; all of these AVF went on to maturation and successful cannulation. Three AVFs were deemed nonsalvageable based on TOF-MR and clinical findings. Two were revised to new accesses and 1 was abandoned as the patient elected for peritoneal dialysis. Two studies were considered nondiagnostic at the time of interpretation. In these two cases, the flow related signal within the vessels was insufficient to produce adequate images. This likely represented failing AVFs with low-flow states that could have been predictive of a non-salvageable AVF. One patient was lost to follow-up.
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All 19 patients in our study had TOF-MRs performed (Table 1). Twelve patients went on to have a conventional catheter angiogram, allowing for intermodality comparison. The congruence rate between the two modalities was 83.3% (Table 2). Cases in which the final report agreed and led to the same intervention were considered congruent. There were 2 false positives identified. In each case the MR overestimated the degree of stenosis.
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Discussion
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This study demonstrated the novel implementation of 3-D TOF-MR in the evaluation of AVF maturation. We found this modality to be useful in avoiding an unnecessary DSA in 21% of our patients. The MRA findings on 4 out of the 19 patients provided information that avoided a diagnostic angiogram. Three of these patients went on to branch ligation without angiogram, and one patient’s AVF was abandoned after MRA showed severe narrowing versus occlusion of the vein. This imaging possessed additional qualitative benefits to other patients, which aided in better case planning, lower radiation exposure, and decreased intravenous contrast amounts. These are similar subjective findings described by Cavagna, et al. in their utilization of MRA on 13 patients with AVF non-maturation.11 The 3-D images provide vessel visualization in multiple planes with a single non-invasive acquisition. We believe this technique delineates the anatomy well and offers several advantages over catheter directed angiography. MR-TOF can obviate the need for invasive access and repeated angiographic runs in multiple planes which frequently leads to increased contrast administration and prolonged radiation exposure.12
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When analyzing CDUS with respect to DSA, the congruence rate was 62%. Reasons for discordant findings included failure to identify the precise location of a stenosis (N = 4) and an unidentified accessory vein branch (N = 1).
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Many studies have shown MRA to benefit in subsequent case planning.13-15 We also found that TOF-MR commonly provided radiologic images that aided in our case preparation. Ten of 12 patients in our group went on to have an angiogram that illustrated concordant findings. The 5
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CDUS remains a valuable tool in the armamentarium of AVF evaluation. However, significant limitations exist, resulting from operator dependence, lack of 3D acquisition, and difficulty displaying complex anatomic and spatial relationships on static images. Sonographic examinations are often limited to the region near the AVF and can miss lesions that the larger field of view obtained with TOF-MR can visualize. Similar to the findings noted by Zhang et al,12 we found that the increased field of view with MRI has tremendous value in evaluating abnormalities that may be more remote than typically identified. One patient in our series had a radial artery stenosis located 10 cm proximal to the anastomosis that was visualized with TOFMR and later treated with conventional angiogram (Figure 2). This lesion would have been likely missed on a standard protocol CDUS.
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TOF-MR can also clarify areas of concern on CDUS and potentially obviate the need for angiography altogether. Two patients had an anastomotic stenosis and several competing veins identified on CDUS. However, subsequent TOF-MR showed the competing veins but no stenosis (Figure 3). If treatment had been based solely on CDUS, both of these patients would have undergone an unnecessary diagnostic angiogram. Instead, both patients underwent venous branch ligation and are now using their AVFs successfully without the need to perform an angiogram.
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There is currently no cost information for AVF TOF-MR, but extrapolating carotid TOF-MR, we estimate it to be about twice the cost of CDUS and one third that of a diagnostic angiogram based on current CHAMPUS National Pricing System reimbursement amounts. Obtaining MRA TOF on all patients prior to intervention is not a cost-effective strategy. Independent of where the DSA is performed, the goals of TOF-MR are to identify cases that could be surgically correctable without DSA, identify potentially non-salvageable AVF, and provide preoperative case-planning for challenging anatomic cases. Further studies designed to refine the criteria that would prompt TOF-MR are needed. Our ultimate goal is to reduce the number of invasive diagnostic procedures while at the same time minimizing unnecessary duplicative diagnostic imaging.
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pre-procedure MRA frequently allowed for decreased contrast administration and immediate lesion identification. One TOF-MR found a venous stenosis that was used as a roadmap to guide percutaneous intervention without the need for contrast administration during venoplasty (Figure 1). We discovered that the TOF-MR frequently provided an anatomic overview which helped plan access site locations near areas of stenosis or served as an anatomic map for future branch vessel ligation.
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During our study, we recognized several limitations of TOF-MR. One potential diagnostic pitfall is the overestimation of the degree of stenosis. Stagnant blood or blood flowing in the same plane as the image acquisition (Figure 4) can also appear as an area of stenosis. Knowledge of 6
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this artifact and interpretation adjustments can mitigate false positive findings on these studies. Relative insensitivity to low flow states can also be a limitation with 3D TOF-MR. Future studies could include 2D TOF-MR in cases were low blood flow is suspected to be the cause for inadequate flow related signal production within vessels. Additionally, velocity and flow rate measurements are currently best obtained with CDUS, but newer phase contrast techniques may offer a promising future for MRI into the physiologic assessment arena. Lastly, given current financial constraints, technological limitations, and the difficulties of treating this chronic population, a pertinent question from this series remains the most appropriate implementation of TOF-MR. We do not argue that every patient warrants this modality following AVF creation. However, our 82% maturation rate in a small study group deemed “at risk” does suggest that there is a role for this in assisting with AVF maturation.
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Conclusion
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3D TOF-MR appears to have significant utility in the evaluation and management of AVF maturation. In addition to demonstrating a high congruence rate with DSA, we found that 21% of patients were spared an unnecessary diagnostic angiogram due to the information provided by TOF-MR. We also felt that, in cases where therapeutic angiogram was indicated, the contrast load and radiation dose was significantly reduced by having a pre-procedure TOF-MR roadmap. Further studies focusing on patient subsets that benefit from TOF-MR will help refine patient selection and may reduce overall costs.
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Our study has several inherent limitations, including the small sample size, single institutional practice, retrospective nature, and qualitative nature. Because we chose to investigate all AVFs which were considered to be at risk for non-maturation, we do not know what the natural history was of this cohort were we not to intervene. However, our results demonstrated that 3D TOF-MR is a feasible imaging modality that has added value in the evaluation of AVF maturation, especially in pre-dialysis patients where contrast exposure is an issue.
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Figure 1. A) TOF-MR image showing tandem stenosis of proximal outflow vein. B and C) DSA with PTA of tandem venous stenosis without intravenous iodinated contrast administration (the contrast is only present within the angioplasty balloon).
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Figure 3. A) TOF-MR image showing a large competing venous branch.
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Figure 4. A) TOF-MR showing an area of decreased signal at the anastomosis interpreted as an area of stenosis. This is a common area of signal loss seen where blood is flowing in the same plane as the image acquisition. B) DSA image showing no significant stenosis.
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Figure 2. A) TOF-MR image showing a proximal arterial stenosis. B) DSA confirming a proximal arterial stenosis.
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Table 1. Patient listing with modality findings and outcomes
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Table 2. 12 cases with TOF-MR and comparison DSA
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Table 3. Outcome of the 7 cases where TOF-MR had no comparison DSA
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References:
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Patel ST, Hughes J, Mills JL. Failure of arteriovenous fistula maturation: An unintended consequence of exceeding Dialysis Outcome Quality Initiative guidelines for hemodialysis access. J Vasc Surg 2003;38:439-45. 4
Doelman C, Duijm LE, Liem YS, et al. Stenosis detection in failing hemodialysis access fistulas and grafts: Comparison of color doppler ultrasonography, contrast-enhanced magnetic resonance angiography, and digital subtraction angiography. J Vasc Surg 2005;42:739-46.
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Ascher E, Gade P, Hingorani A, et al. Changes in the practice of angioaccess surgery: Impact of dialysis outcome and quality initiative recommendations. J Vasc Surg 2000;31:84-92.
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Dumars MC, Thompson WE, Bluth EI, et al. Management of suspected hemodialysis graft dysfunction: Usefulness of diagnostic US. Radiology 2002;222:103-7. 6
Tordoir JH, DeBruin HG, Hoeneveld H, et al. Duplex ultrasound scanning in the assessment of arteriovenous fistulas created for hemodialysis access: Comparison with digital subtraction angiography. J Vasc Surg 1989; 10: 122-8. 7
Middleton WD, Picus DD, Marx MV, et al. Color Doppler sonography of hemodialysis vascular access: Comparison with angiography. Am J Roentgenol 1989; 152: 633-39. 8
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Waldman GJ, Pattynama PM, Chang PC, et al. Magnetic resonance angiography of dialysis access shunts: Initial results. Magn Reson Imaging 1996; 14(2):197-200. 9
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Konermann M, Sanner B, Laufer U, et al. Magnetic resonance angiography as a technique for the visualization of hemodialysis shunts. Nephron 1996;73:73-8. 10
Robbin ML, Chamberlain NE, Lockhart ME, et al. Hemodialysis arteriovenous fistula maturity: US evaluation. Radiology 2002;225:59-64. 11
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National Kidney Foundation. K/DOQI clinical practice guidelines for vascular access, 2000. Am J Kidney Dis 2001;37:S137-S81.
Cavagna E, D’Andrea P, Schiavon F, et al. Failing hemodialysis arteriovenous fistula and percutaneous treatment: imaging with CT, MRI and digital subtraction angiography. Cardiovasc Intervent Radiol 2000;23:262-5. 12
Zhang J, Hecht E, Maldonado T, et al. Time-resolved 3D angiography with parallel imaging for evaluation of hemodialysis fistula and grafts: Initial experience. Am J Roentgenol 2006;186:1436-42.
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Froger CL, Duijm LE, Liem YS, et al. Stenosis detection with MR angiography and digital subtraction angiography in dysfunctional hemodialysis access fistulas and grafts. Radiology 2005;234:284-91. 15
Planken RN, Tordoir JH, Dammers R, et al. Stenosis detection in forearm hemodialysis arteriovenous fistulae by multiphase contrast-enhanced magnetic resonance angiography: Preliminary experience. J Magn Reson 2003;17:54-64.
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Smits JH, Bos C, Elgersma OE, et al. Hemodialysis access imaging: Comparison of flowinterrupted contrast-enhanced MR angiography and digital subtraction angiography. Radiology 2002;225:829-34.
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Angiogram / Intervention Anastomotic & venous stenosis / PTA Branch ligation Unremarkable Venous stenosis N/A Venous stenosis & competing vein / PTA & branch ligation Anastomotic & venous stenosis / PTA N/A PTA & Branch ligation in OR N/A Branch ligation Competing vein / branch ligation Anastomotic stenosis / PTA Venous stenosis / PTA Venous & arterial stenosis / PTA Venous stenosis / PTA N/A Anastomotic stenosis & competing vein / PTA Thrombosis AVF / tPA & PTA
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Time-of-Flight MR Anastomotic & venous stenosis Competing veins Anastomotic stenosis Venous stenosis Non-diagnostic exam Venous stenosis Anastomotic & venous stenosis Venous stenosis & competing veins Venous stenosis & competing veins Non-diagnostic exam Competing veins Venous stenosis & competing vein Anastomotic stenosis Venous stenosis Venous & arterial stenosis Venous stenosis Severe narrowing vs occlusion of vein Anastomotic stenosis & competing vein Venous stenosis
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Color-flow Duplex Ultrasound Arterial stenosis Arterial stenosis & competing vein Low flow Anastomotic stenosis Anastomotic stenosis & competing veins N/A Venous stenosis Anastomotic stenosis Competing veins & low flow N/A Anastomotic stenosis & competing veins Anastomotic stenosis Proximal venous stenosis Venous stenosis Venous & arterial stenosis Venous stenosis N/A Anastomotic stenosis & competing vein N/A
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Outcome Mature Successful use Mature Pt expired New access Successful use Successful use Lost to f/u Mature New access Successful use Mature Mature Successful use Successful use Successful use Abandoned Successful use Successful use
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Table 2. 12 cases with TOF-MR and comparison DSA
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Intervention PTA PTA PTA/branch ligation PTA PTA PTA PTA PTA PTA tPA / PTA Branch ligation -
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Angiogram Same Same Same Same Same Same Same Same Same Thrombosis AVF Competing vein Unremarkable
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Time-of-Flight Magnetic Resonance Anastomotic & venous stenosis Venous stenosis Venous stenosis & competing veins Anastomotic & venous stenosis Anastomotic stenosis Venous stenosis Venous & arterial stenosis Venous stenosis Anastomotic stenosis & competing vein Venous stenosis Venous stenosis & competing vein Anastomotic stenosis
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Table 3. Outcome of the 7 cases where TOF-MR had no comparison DSA
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Intervention Branch ligation (OR) PTA & branch ligation (OR) Branch ligation (OR) N/A N/A N/A N/A
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Time-of-Flight Magnetic Resonance Competing veins Venous stenosis & competing veins Competing veins Severe narrowing vs occlusion of vein Non-diagnostic exam Non-diagnostic exam Venous stenosis & competing veins
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Outcome Successful use Successful use Successful use Peritoneal dialysis New access New access Lost to follow-up
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